Construction began almost immediately after the purchase of the building, and was shrouded in secrecy until visitors were first allowed into the museum to see the work in progress on New Year's Eve 1996.

With the construction of the iconic giant whale in the lobby completed in 1997, the museum opened to the public on October 25 of the same year.

[5] The museum has regularly expanded, adding new exhibits such as MonstroCity in 2002, Enchanted Caves and Shoe Shaft in 2003, and World Aquarium in 2004.

The building's fifth floor consists of apartments, dubbed the Lofts at City Museum, which range in size from 1,300 to more than 2,800 square feet (260 m2).

[6] The original part of the museum, the first floor is home to a life-size Bowhead Whale that guests can walk through to view a large fish tank from the mezzanine.

Also on the first floor are a number of tunnels that run across the ceiling, hiding above a sea of aircraft Kevlar cut to give the impression of icicles.

It housed a variety of animals such as sharks, rays, sea turtles, parrots, tortoises, terrapins, otters, snakes, alligators and sloths as well as freshwater and saltwater fish.

The World Aquarium portion of the City Museum closed on September 7, 2015, and relocated to Laclede's Landing, St. Louis,[7] before eventually shutting down several years later.

Beatnik Bob's is directly across from the Circus, which features the "World's Largest Underwear" (a pair of men's briefs that are about seven feet high and seven feet wide), a collection of vintage video and pinball games, and a concessions stand, bar and coffee shop.

The pond fountain, which once had stepping stones that connected one side to the other, has now been covered with astroturf with future plans unknown.

A 24-foot metal praying mantis stands atop a dome salvaged from the St. Louis Science Center during its remodeling.

Originally the home of the son of Daniel Boone, it was owned by the Hezel family for more than a century and is now a bar and entertainment venue.